EAST RUTHERFORD, N.J. — Tom Coughlin’s smile in the aftermath of Sunday’s loss to the Philadelphia Eagles might have been the biggest tip-off of what was to come.

For his 12 years as the Giants’ coach — and probably for the 34 years he had coached previously — it took a lot to get Coughlin to smile in public after a defeat. But on Sunday, a reporter brought up Coughlin’s 11 grandchildren, who were on the sidelines for what turned out to be his last game with the Giants, and the 69-year-old Coughlin could not help himself.

Suddenly appearing relieved, he burst into a wide grin.

Coughlin stepped down as coach about 22 hours later. After meeting with ownership Monday afternoon, Coughlin chose the dignified exit instead of being forced out after three consecutive losing seasons. While the move was not surprising, it brings an end to a prosperous era in the franchise’s history that included two Super Bowl victories and five playoff appearances.

Coughlin smiled on his way out, but it does not mean the Giants’ losing ways and manifold problems will depart with him.

The team’s roster is missing talent and depth — not a good combination — at all but a handful of positions. Some parts of the team are aging and injury-prone, and others are green with inexperience. Psychologically, a losing mentality has set in, which was repeatedly evident this season as the Giants lost leads in the final 75 seconds of games an unfathomable six times.

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A tearful Eli Manning said of Coughlin, "He definitely has not failed these players. We failed him."CreditRichard Perry/The New York Times

The Giants also had the N.F.L.’s worst defense, a sector of the team that was only tangentially under the purview of the offense-minded Coughlin. On defense, the Giants did not have a single player whom opposing coaches fretted about as they prepared their offensive game plans.

Although Jerry Reese, the Giants’ general manager, drafted the star receiver Odell Beckham Jr. two years ago, dozens of Reese’s draft selections in the last eight years have been busts, which has left the Giants with gaping deficiencies at safety, linebacker and tight end and on the defensive line. Without a core of homegrown players, the Giants have turned to free agency to buttress the roster, but their acquisitions have failed to get the team into the playoffs since the 2011 season.

The co-owner John Mara was unafraid to characterize this season as a win-or-else situation after the Giants went 6-10 in 2014. But a year later, the Giants’ record was no different.

That sealed Coughlin’s fate, and he was gracious as he departed, issuing a statement in which he said he was stepping down in the best interests of the team and his family.

“It has been an honor and a privilege to serve as head coach of the New York Football Giants,” Coughlin said. “This is not a sad occasion for me.”

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Defensive end Jason Pierre-Paul spoke to the news media.CreditRichard Perry/The New York Times

Coughlin continued, “Obviously, the past three years have not been what any of us expect, and as head coach, I accept the responsibility for those seasons.”

Interestingly, Coughlin did not retire from coaching, as many suspected he might. He will immediately become a candidate for several vacant N.F.L. jobs and could be staring across the field at the Giants from an opposing sideline in nine months.

One of the N.F.L.’s most successful coaches, especially in the modern era, Coughlin coached in Jacksonville before joining the Giants in 2004 and has a career N.F.L. record of 170-150, with a 12-7 mark in playoff games. He was 102-90 with the Giants in the regular season and 8-3 as their coach in the postseason.

For Giants fans, Coughlin will be best remembered for his upset victories over the New England Patriots in Super Bowls after the 2007 and 2011 seasons. Although not popular with fans or members of the media after his first three seasons, Coughlin reworked his image and approach and grew to become the crafty face of underdog, unrecognized teams.

After the 2007 regular season, the Giants won three consecutive road playoff games and then upset the previously unbeaten Patriots in Super Bowl XLII, 17-14.

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Giants players cleaned out their lockers Monday after they finished with a losing record for the third straight season.CreditRichard Perry/The New York Times

The Giants were 30-18 in their next three seasons but did not win a playoff game. They sneaked into the playoffs with a 9-7 record at the end of the 2011 season and were once again pitted against the Patriots in the Super Bowl. The Giants won in another upset, 21-17.

Where the Giants will turn for their next coach will be a quandary for management, which likes to hire experienced head coaches, especially ones with Giants ties who have something to prove. New Orleans Coach Sean Payton is a former Giants assistant, but he is under contract and would fetch serious compensation. There are young candidates who would most likely jump at the chance to take over the storied Giants, and several of them are respected offensive coordinators with other N.F.L. teams: Chicago’s Adam Gase, New England’s Josh McDaniels and Carolina’s Mike Shula. None of those three, however, have direct Giants ties or lengthy — or successful — head coaching experience.

There are accomplished college coaches who might draw interest, including David Shaw of Stanford and Notre Dame’s Brian Kelly. But a college coach trying to graduate to the N.F.L. would probably not be the Giants’ style.

One of the Giants’ first, most significant decisions is going to be figuring out what to do with Coughlin’s offensive coordinator, Ben McAdoo, and his defensive coordinator, Steve Spagnuolo, who is well liked by management but failed to win as the St. Louis Rams’ head coach several years ago.

McAdoo has no head coaching experience, but under his tutelage in the last two seasons, Eli Manning has flourished. This season, Manning threw 35 touchdowns with only 14 interceptions.

More impressive, the Giants ranked sixth in the N.F.L. in points this season and eighth in yards.

“I feel very comfortable in the offense,” Manning said Monday, as he also choked back tears talking about his last meeting with Coughlin.

If McAdoo is not promoted, or a new coach brings in his own offensive coordinator, which is common, it will mean that Manning will be working in his third offensive system in the last four years.

Asked about the difficulty of that situation, Manning responded: “Obviously, it would not be ideal. But I’ll handle it.”

Manning’s expression betrayed his true emotions. He turned 35 years old Sunday and is not looking forward to starting all over in a new offense.

But that is just another one of the many dilemmas facing the Giants’ management in the first days of the post-Coughlin era.

Reese, Mara and the co-owner Steve Tisch will appear at a news conference Tuesday morning, presumably to explain how the browbeaten Giants plan to regain their place among the N.F.L.’s elite.

Coughlin is going to be there, too. He will no doubt be smiling. It’s not his problem any longer.

A version of this article appears in print on , Section B, Page 8 of the New York edition with the headline: Giants Close Door on Era, Ushering In Uncertainty. Order Reprints | Today’s Paper | Subscribe